Cyclical Generation and Degeneration of Organs in a Colonial Urochordate Involves Crosstalk between Old and New: A Model for Development and Regeneration

[摘要] Botryllusschlosseriisacolonialmarineurochordateinwhichalladultorganisms(calledzooids)inacolonydiesynchronouslybyapoptosis(programmedcelldeath)incyclicalfashion.Duringthisdeathphasecalledtakeover,cellcorpseswithinthedyingorganismareengulfedbycirculatingphagocyticcells.The“old”zooidsandtheirorgansareresorbedwithin24–36h(programmedcellremoval).Thisprocesscoincidestemporallywiththegrowthofasexuallyderivedprimarybuds,thatharborasmallnumberofundifferentiatedcells,intomaturezooidscontainingfunctionalorgansandtissueswiththesamebodyplanasadultzooidsfromwhichtheybudded.Withinthesecolonies,allzooidssharearamifyingnetworkofextracorporealbloodvesselsembeddedinagelatinoustunic.Theunderlyingmechanismsregulatingprogrammedcelldeathandprogrammedcellremovalinthisorganismareunknown.Inthisstudy,weextirpatedbudsorzooidsfromB.schlossericoloniesinordertoinvestigatetheinterplaythatexistsbetweenbuds,zooids,andthevascularsystemduringtakeover.Ourfindingsindicatethat,inthecompleteabsenceofbuds(budectomy),organsfromadultzooidsunderwentprogrammedcelldeathbutweremarkedlyimpairedintheirabilitytoberesorbeddespiteengulfmentofzooid-derivedcellcorpsesbyphagocytes.However,whenbudswereremovedfromonlyhalfoftheflower-shapedsystemsofzooidsinacolony(hemibudectomy),thebudectomizedzooidswerecompletelyresorbedwithin36–48hfollowingonsetofprogrammedcelldeath.Furthermore,ifhemibudectomieswerecarriedoutbyusingsmallcolonies,leavingonlyasinglefunctionalbud,zooidsfromtheoldgenerationwerealsoresorbed,albeitdelayedto48–60hfollowingonsetofprogrammedcelldeath.Thisbudeventuallyreachedfunctionalmaturity,butgrewsignificantlylargerinsizethananycontrolzooid,andexhibitedhyperplasia.Thisfindingstronglysuggestedthatcomponentsofthedyingzooidvisceracouldbereutilizedbythedevelopingbuds,possiblyaspartofacolony-widerecyclingmechanism.Inordertotestthishypothesis,zooidsweresurgicallyremoved(zooidectomy)attheonsetoftakeover,andbudgrowthwasquantitativelydetermined.Inthesezooidectomizedcolonies,budgrowthwasseverelycurtailed.Inmostsolitary,long-livedanimals,organsandtissuesaremaintainedbyprocessesofcontinualdeathandremovalofagingcellscounterbalancedbyregenerationwithstemandprogenitorcells.InthecolonialtunicateB.schlosseri,thesamekindsofprocessesensurethelongevityofthecolony(ananimal)bycyclesofdeathandregenerationofitsconstituentzooids(alsoanimals).

[学科分类] 生物科学（综合）

[关键词] ascidian;urochordate;apoptosis;programmed cell death;Botryllus;phagocytes;recycling